Evolution of Cutaneous Sugar Transport Functions in Proterometra dickermani (Digenea: Azygiidae)

Abstract

Cercariae of Proterometra dickermani grow to fully mature adults in tissues of its snail host. Although adults are known to absorb glucose by Na+dependent active transport, we found that glucose uptake by cercariae was Na+-independent. Cercarial transport also was insensitive to phlorizin, but it was inhibited by phloretin indicating facilitated diffusion, the type of transport found in both cercariae and gutdwelling adults of Proterometra macrostoma and Proterometra edneyi. Thus, active transport in the adult of P. dickermani is interpreted as a secondary specialization consistent with the known sugar transport capacities of other tissue-dwelling digeneans. Most species of Proterometra use a snail and a fish host in their life cycles. There is no metacercarial stage because furcocystocercous cercariae emerging from snails possess in utero embryos in early cleavage stages. After the free-swimming cercariae are ingested by fish, the cercarial bodies leave the tails and complete development. Adults are usually found in the fish stomach [e.g., Proterometra edneyi, Uglem and Aliff (1984)], but those of Proterometra macrostoma can live also on external surfaces of the pharynx and gills (Horsfall, 1933). Proterometra dickermani does not require a fish host in its life cycle; adult worms are found in the same snails that produce cercariae (Anderson and Anderson, 1963). Adults of Proterometra spp. also differ in their cutaneous sugar transport capacities (Uglem et al., 1985). Facilitated diffusion is the type of transport in gut-dwelling adults of P. macrostoma and P. edneyi; however, this capacity disappears in the ectoparasitic forms of P. macrostoma (Uglem, 1980, 1987). By contrast, adults of P. dickermani, which are tissue-dwellers, take up glucose by active transport. Because facilitated diffusion is the type of transport expressed in cercariae of P. macrostoma and P. edneyi, it seemed desirable to determine which type is expressed in cercariae of P. dickermani. Consequently, we describe the ontogeny of cutaneous sugar transport functions in P. dickermani and compare it with that of P. macrostoma and P. edneyi. Snails of the species Goniobasis livescens were collected from Oqueoc River in Presque Isle County, Michigan. Snails were transported to the laboratory, crushed in artificial snail water (ASW; 50 mM NaCl, 1.0 mM KC1, 5.0 mM CaCl2, 0.5 mM MgCl2), and examined for secondary germinal sacs and adults of P. dickermani that can be distinguished readily from its congeners (Anderson, 1962; Uglem and Aliff, 1984). No other species of Proterometra was present. Germinal sacs were dissected carefully with fine needles to obtain cercariae. Specimens were flattened slightly under coverslips and examined with the aid of a dissecting microscope. All in utero eggs in cercariae were undeveloped. In adults some eggs contained fully developed miracidia. Bodies were mechanically separated from their tails and randomized into groups of 4 or 5. Uptake of 0.025 mM D-[6-3H]glucose (1 mCi/,tmole; Amersham Corp.) in ASW by groups of cercarial bodies in replicates of 4 was determined using the glucose transport inhibitors and methods as described previously (Uglem et al., 1985). Differences were analyzed using the Student's t-test with a value of P < 0.05 considered significant. Active transport of glucose by adults of P. dickermani is known to be Na+-dependent and more sensitive to the inhibitor phlorizin than to phloretin (Table I). However, transport by cercariae was insensitive to Na+ and phlorizin and inhibited completely by phloretin indicating facilitated diffusion. Because neither cercarial nor adult transport was partially sensitive to Na+, the 2 types of transport are expressed independently. Glucose uptake by immature cercariae (no eggs in utero) was unaffected by unlabeled glucose or the inhibitors in Table I (data not shown) indicating simple diffusion. Niche segregation in Proterometra spp. and other digeneans involves the differential expression of the 2 types of sugar transport (Uglem et al., 1985). Species from the lumen of the alimentary canal or associated organ take up glucose by facilitated diffusion, whereas active This content downloaded from 207.46.13.111 on Tue, 09 Aug 2016 06:17:27 UTC All use subject to http://about.jstor.org/terms 466 THE JOURNAL OF PARASITOLOGY, VOL. 75, NO. 3, JUNE 1989